BioMed Central Page 1 of 6 (page number not for citation purposes) Journal of Brachial Plexus and Peripheral Nerve Injury Open Access Research article Variations of the origin of collateral branches emerging from the posterior aspect of the brachial plexus Luis Ernesto Ballesteros* and Luis Miguel Ramirez Address: Medicine Faculty, Universidad Industrial de Santander, Bucaramanga, Colombia Email: Luis Ernesto Ballesteros* - lballest56@yahoo.es; Luis Miguel Ramirez - lmra3@yahoo.com * Corresponding author Abstract Background: The frequency of variation found in the arrangement and distribution of the branches in the brachial plexus, make this anatomical region extremely complicated. The medical concerns involved with these variations include anesthetic blocks, surgical approaches, interpreting tumor or traumatic nervous compressions having unexplained clinical symptoms (sensory loss, pain, wakefulness and paresis), and the possibility of these structures becoming compromised. The clinical importance of these variations is discussed in the light of their differential origins. Methods: The anatomy of brachial plexus structures from 46 male and 11 female cadaverous specimens were studied. The 40–80 year-old specimens were obtained from the Universidad Industrial de Santander's Medical Faculty's Anatomy Department (dissection laboratory). Parametric measures were used for calculating results. Results: Almost half (47.1%) of the evaluated plexuses had collateral variations. Subscapular nerves were the most varied structure, including the presence of a novel accessory nerve. Long thoracic nerve variations were present, as were the absence of C5 or C7 involvement, and late C7 union with C5–C6. Conclusion: Further studies are needed to confirm the existence of these variations in a larger sample of cadaver specimens. Background Brachial plexus (BP) anatomical variations have been described in humans by many authors, although such var- iations have not been extensively catalogued [1-4]. Varia- tions in plexus patterns may be due to unusual formation during the development of trunks, divisions, or cords [5]. The more common BP variations occur at the junction or separation of the individual parts [6,7]. Peripheral (collat- eral) nerves arise from the whole plexus trajectory. These collaterals reach proximal regions exclusively innervating some scapular belt muscles. Anesthetic blocks, surgical approaches, the interpretation of a nervous compression having unexplained clinical symptoms (sensory loss, pain, wakefulness and paresis), and these structures being compromised represent the clinical importance of these variations [8,9]. Dorsal scapular, long thoracic, suprascapular, subscapularis and Published: 23 June 2007 Journal of Brachial Plexus and Peripheral Nerve Injury 2007, 2:14 doi:10.1186/1749-7221-2- 14 Received: 18 February 2007 Accepted: 23 June 2007 This article is available from: http://www.JBPPNI.com/content/2/1/14 © 2007 Ballesteros and Ramirez; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0 ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Journal of Brachial Plexus and Peripheral Nerve Injury 2007, 2:14 http://www.JBPPNI.com/content/2/1/14 Page 2 of 6 (page number not for citation purposes) thoracodorsal origins were studied to show variable BP collateral arrangements. Methods BP structures from 46 male and 11 female mixed-race, cadaverous specimens (40–80 years old) were studied. These specimens were obtained from the Medical Fac- ulty's Department of Anatomy (dissection laboratory) at Universidad Industrial de Santander during academic semesters in 2005 and 2006. The cause of death for each cadaver was not known in detail. The specimens enter the dissection laboratory as donated material which relatives have not claimed from the University Hospital. None of them had suffered pathological lesions, traumatic lesions or surgical procedures in the neck, thoracic or axillary region. All specimens were fixed in 10% formaldehyde solution. The dissections were performed by the authors involving three specific areas: neck, antero-lateral thorax and delto-scapular area. The origin of the BP collaterals were carefully dissected from the cervico-thoracic roots to the final muscular innervation contact. Dorsal scapular, long thoracic, suprascapular, subscapularis and thoraco- dorsal nerves were dissected separately at the end of the procedure. Pectoralis medial and lateral branches, and the subclavian nerve were not included due to difficulty of accessing the posterior aspect of the BP. This included the first plane of dissection that involved pectoralis major and minor muscles and the clavicle with its respective innerva- tion. Each finding was ordered, photographed, and regis- tered according to gender, side, level of union and collateral origin, and the presence of additional collater- als. The results were descriptive, and data was presented as absolute numbers and percentages. The origin of each studied nerve was categorized as having a usual origin (illustrated in classical texts) or a variation (Table 1, Table 2). Results We found that 33.9% of upper subscapular nerves, 31.6% of lower subscapular nerves, 78.6% of thoracodorsal nerves, 20.4% of long thoracic nerves, 82.4% of supras- capularnerves and 17.9% of dorsal scapular nerves had the usual origins expected for BP collaterals. Tables 1, 2 and 3 show the variations, summarizing all collateral ori- gin variations in an ordered form. Variations were not bilateral in any cadaver. The most variable structures are seen in Figures 1, 2, 3, 4. Briefly, 54.4% of the lower sub- scapular nerves originated from the axillary nerve and 12.3% from the thoracodorsal nerve (Fig 1). 50% of the upper subscapular nerves originated from the posterior division (PD) of the superior trunk (ST) (Fig 2), 5.4% from the axillary nerve, and 3.6% from the union of the ST and middle trunk (MT) (Table 1). Other variations included a common C5 nerve ramus forming the long thoracic and dorsal scapular nerves (35.2%) (Table 2; Fig 3), a late union below the first rib from C7 with C5–C6 forming the long thoracic nerve (33.3%), a suprascapular nerve originating from the C5 ventral ramus (15.8%), a thoracodorsal nerve originating from the radial nerve (8.9%), an accessory subscapular nerve in 38.7% of the samples (Fig 4), and the accessory subscapular nerve was observed coming from the posterior cord in 21.1% of the samples. There were no significant differences regarding gender or side where the variations were found (p = 0.876 and 0.523, respectively). Table 2: Frequency of origins of long thoracic, suprascapular and dorsal scapular nerves. Long thoracic n (%) From C5, C6, C7 -above the 1 st rib (early union) – (usual) 11 (20.4) From C5, C6, C7 -above the 3 rd rib (late union) 6 (11.1) C5 (dorsal scapular common trunk), C6, C7-(early union) 7 (13.0) C5 (dorsal scapular common trunk), C6, C7-(late union) 12 (22.2) C5 not supplying 6 (11.1) C7 not supplying 10 (18.5) without union (C5, C6 + C7/C5 + C6, C7) 2 (3.7) Suprascapular n (%) From ST (usual) 47 (82.4) From C5 9 (15.8) From C5 and ST 1 (1.8) Dorsal scapular n (%) From unique ramus (usual) 10 (17.9) From common trunk with long thoracic 17 (30.4) From C4 16 (28.6) From C4, C5 13 (23.1) Table 1: Frequency of subscapular nerves origins. Upper subscapular n (%) From posterior cord (usual) 19 (33.9) From axillary 3(5.4) From PD of ST 28 (50) From ST and MT 2 (3.6) From others: suprascapular or C8 4 (7.1) Lower subscapular n (%) From posterior cord (usual) 18 (31.6) From axillary 31 (54.4) From radial 1 (1.7) From thoracodorsal 7 (12.3) Thoracodorsal n (%) From posterior cord (usual) 44 (78.6) From radial 5 (8.9) From MT 2 (3.6) From axillary 5 (8.9) Accessory subscapular n (%) From posterior cord 12 (21.1) From ST 6 (10.6) From axillary 4 (7) Absent 35 (61.3) Journal of Brachial Plexus and Peripheral Nerve Injury 2007, 2:14 http://www.JBPPNI.com/content/2/1/14 Page 3 of 6 (page number not for citation purposes) Discussion BP variations regarding collateral branches are common, but have not been fully reported in several investigations. These results reinforce the concept that anatomical varia- tions are so common that normal textbook parameters must be treated carefully, especially regarding surgical procedures. Uzun et al. [10] have stated that BP variations could be prevented during extensive surgical procedures in the neck and axilla which are considered vulnerable areas involving legal repercussions [11,12]. Uysal et al. [13] found 53.5% of human fetuses have different varia- tions in the BP. Our results were similar in that 47.1% of the evaluated plexuses had collateral variations. Regard- ing side and gender, controversial results have been returned due to Uysal et al. [13] and Kerr [14] affirming that variations were more likely in females and on the right-hand side. However, Uzun et al. [10] and Fazan et al. [15] found no differences. Our results revealed no discrep- ancy concerning this variable. A classical description of the long thoracic nerve (LTN) deals with a nerve formed by an upper portion originating from C5 and C6 nerve roots and a lower portion coming from C7. The union of the upper and lower portions are normally linked to either the axilla (an extensive, not well-discriminated area) or the upper border of the ante- rior serratus muscle (first rib). Tubbs et al. [16] found that 61% of cadaverous specimens had C5, C6 and C7 union at the second rib posterior to the axillary artery. They also found this union was at the first rib level posterior to the MT of the BP in 33% of cases. In addition, they also found that the C5 element of the LTN did not join with C6 and C7 and traveled directly to the serratus anterior muscle in 6% of cases. We found this same component in 3.7% of our samples. Several surgical procedures including first rib resection, lung surgery, transaxillary thoracotomy, and chest tube placement might cause injury to the long thoracic nerve [4,17]. Our results showed a significant late union in 18 cases (33.3%). This might explain partial lesions in a patient's clinical symptoms when these nerves are injured, resulting in such morphological expression. A detailed Right BP with collateral origin variations for lower subscapu-lar nerve and thoracodorsal nerveFigure 2 Right BP with collateral origin variations for lower subscapu- lar nerve and thoracodorsal nerve. C4, C5, C6, C7, C8, T1, T2: spinal nerve ventral rami with prefixed C4 (asterisk) and postfixed T2 (asterisk). ST: superior trunk. MT: middle trunk. IT: inferior trunk. LC: lateral cord. PC: posterior cord. MC: medial cord. A: axillary nerve. R: radial nerve. Mct: musculo- cutaneous nerve. U: ulnar nerve. M: median nerve. ASM: ser- ratus anterior muscle. SSM: subscapularis muscle. CP: cervical plexus. 1: dorsal scapular nerve (originating from C4). 2: suprascapular nerve. 3: upper subscapular nerve. 4: lower subscapular nerve (originating from the axillary nerve). 5: thoracodorsal nerve originating from MT posterior divi- sion. 6: long thoracic nerve. Table 3: Percentage of BP collateral origins (usual and variable presentation). BP collateral Usual n (%) Variation n (%) Long thoracic 18 (33.3) 36 (66.6) Suprascapular 47 (82.5) 10 (17.5) Dorsal scapular 27 (48.2) 29 (51.8) Upper subscapular 19 (33.9) 37 (66.1) Thoracodorsal 44 (78.6) 12 (21.4) Inferior subscapular 18 (31.6) 39 (68.4) Accessory subscapular 35 (61.4)* 22 (38.6) *Absent collateral (usual) Right BP with collateral origin variations for upper subscapu-lar nerve and an accessory subscapular nerveFigure 1 Right BP with collateral origin variations for upper subscapu- lar nerve and an accessory subscapular nerve. C5, C6, C7, C8, T1: spinal nerve ventral rami. ST: superior trunk. MT: middle trunk. IT: inferior trunk. LC: lateral cord. PC: poste- rior cord. MC: medial cord. A: axillary nerve. R: radial nerve. Mct: musculocutaneous nerve. U: ulnar nerve. M(LH): lateral head of median nerve. M(MH): medial head of median nerve. PM: pectoralis minor muscle. SSM: subscapularis muscle. DM: deltoid muscle. 1: dorsal scapular nerve.2: suprascapular nerve. 3: upper subscapular nerve (originating from the ST posterior cord). 4: accessory subscapular nerve. 5: lower subscapular nerve. 6: long thoracic nerve. Journal of Brachial Plexus and Peripheral Nerve Injury 2007, 2:14 http://www.JBPPNI.com/content/2/1/14 Page 4 of 6 (page number not for citation purposes) picture of upper and lower portion union (late or proxi- mal) must thus be provided to avoid damage by a surgeon who counts on such description. Familiarity with a varia- tion's origin and the trajectory of collateral nerves emerg- ing from the posterior aspect of the BP (i.e. subscapularis and thoracodorsal) must be taken into account by a sur- geon during procedures such as radical mastectomy with axillary emptying to prevent unfavorable iatrogenic out- comes. Besides the presence of an accessory subscapular nerve, understanding the late or lateral origin of a collat- eral nerve emerging from radial or axillary nervesis vital for evading positive motor signs, such as compromising arm adduction, extension or medial rotation. Moreover, C5 (11%) and C7 (18%) do not always con- tribute to the long thoracic nerve. Lee et al. [18] found that C5 (11.3%) and C7 (7.7%) were not necessarily contrib- uting components. Horwitz and Tocantins [19] and Hov- elacque [20] found the C7 component of the LTN absent in 8% and 1.7% of cases, respectively. Although other studies found additional contributions from C4 and C8 to the LTN in a small number of cases, we could not identify them in this study [18,19,23]. Our results regarding the dorsal scapular nerve fit the clas- sical description of originating from C5 in only 48.3% of the samples. We also found an origin from a common trunk with the LTN (30.4%) in fewer cases than Horwitz and Tocantis [19] (44%). Interestingly, Lee et al. [18] described a classical dorsal scapular nerve in 75.8% of the samples, as well as finding a variation spectrum consisting of 9% originating from ST, 7.6% from C4, C5 and 7.6% from C6. Tubbs et al. found dorsal scapular nerve originat- ing from C5 in 95% of cases and the rest from C5, C6 spi- nal nerves [21]. Mallesy et al. confirmed the additional cervical plexus supply (C3, C4) to the levator scapula muscle, just as anatomical textbooks state [22]. Interest- ingly, Yan et al. stress the real and apparent origins of spi- nal BP segments, detailed work showing an additional source of upper spinal segment fibers to the BP and their anterior and posterior arrangement refuting macroscopic BP arrangement [23]. Regarding the suprascapular nerve, we found little varia- tion from the classical description (82.4%). Lee et al. [18] found it originating from C5 in one case, and Fazan et al. [14] found the same origin in 5.5% of cases. Lee et al. [18] also found the suprascapular nerve originating from C6 (1.3%) and C4 contributing to C5 (7.2%). Yan et al. showed that anterior and posterior contributions form the spinal segment of the BP to the suprascapular nerve [24]. We believe that the most rostral motor contribution (C4) Left BP with collateral origin variations for subscapular nervesFigure 4 Left BP with collateral origin variations for subscapular nerves. C5, C6, C7, C8, T1: spinal nerve ventral rami. ST: superior trunk. MT: middle trunk. IT: inferior trunk. LC: lat- eral cord. PC: posterior cord. MC: medial cord. A: axillary nerve. R: radial nerve. Mct: musculocutaneous nerve. U: ulnar nerve. M: median nerve. ASM: serratus anterior muscle. SSM: subscapularis muscle. PMM: pectoralis minor muscle. 1. suprascapular nerve. 2: upper subscapular nerve (originating from the ST posterior cord). 3: accessory subscapular nerve. 4. lower subscapular nerve (originating from the thoracodor- sal nerve). 5: long thoracic nerve. 6: dorsal scapular nerve (originating from C4). Left BP with collateral origin variations for shared C5Figure 3 Left BP with collateral origin variations for shared C5. C5, C6, C7, C8, T1: spinal nerve ventral rami. AA: axillary artery. LSM: levator scapula muscle. SSM: subscapular muscle. ASM: anterior serratus muscle. A: axillary nerve. R: radial nerve. U: ulnar nerve. M: median nerve.1: dorsal scapular nerve. 2: ramus from C5 to long thoracic (sharing the same root with dorsal scapular). 3: C6 ramus to long thoracic. 4: suprascapu- lar nerve. 5: upper subscapular nerve. 6: lower subscapular nerve. 7: thoracodorsal nerve. 8: long thoracic nerve. Journal of Brachial Plexus and Peripheral Nerve Injury 2007, 2:14 http://www.JBPPNI.com/content/2/1/14 Page 5 of 6 (page number not for citation purposes) to this nerve might be consistent with a shared lesion when this medullar segment is involved with a biome- chanical effect on shoulder mobility and diaphragmatic function (phrenic nerve). The thoracodorsal nerve originated from the posterior cord (PC) in 78.6% of samples in the present study. A clas- sical description of the thoracodorsal nerve origins involves three different origins including the MT (3.6%), radial (8.9%), and axillary (8.9%) nerves. Fazan et al. [15] found an axillary origin or a radial nerve origin in 13% and 5.5% of cases, respectively. Tubbs et al. found 1.5% of thoracodorsal nerves coming from the radial nerve [25]. Trauma of the posterior wall of the axillary region could harm latisimus dorsis muscle function (humeral move- ment extension, adduction and medial rotation), depend- ing on lesion level and the involvement of its several origins. For instance, an axillary nerve lesion engaging the thoracodorsal nerve origin may produce a more extensive functional lesion including latisimus dorsi, deltoid and teres minor muscles. The upper subscapular nerve presented broad variability in our findings. The most frequent result did not fit the classical description of a PC origin in 50% of the cases. We found 33.9% originating from the PC and the rest from axillary, suprascapular and C8 spinal nerves. Lee et al. [18] considered upper subscapular nerves originating from the axillary nerve to be very infrequent. However, Fazan et al. [15] observed an axillary origin in 5.5% of cases and Tubbs et al. [26] found it in 3%, which was similar to our results. Even though Tubbs et al. [26] reported that the lower sub- scapular nerve originates directly from the axillary nerve's proximal segment, we found this late origin in only 54.4% of samples. This is in agreement with Fazan et al. who found this at a rate of 54% [15]. Although Lee et al. [18] only observed occasional lower subscapular nerve sources coming from the thoracodorsal nerve, we found 12% of this configuration in our study and Fazan et al. observed 7% as well [15]. Among several findings in some of the BP collaterals, the present study confirms the existence of the accessory sub- scapular nerve. Even though this nerve has been noted in previous studies, none of them have classified it or calcu- lated its incidence (38.7%), originating mostly from the posterior cord (21.1%). There must be full awareness of the origin of variation in collateral branches from the posterior aspect of the BP and their configuration due to their significance in interpret- ing diagnostic images, nerve blocks, traumatic damage and surgical approaches. Unexplained clinical symptoms, such as sensory loss, pain, wakefulness and paresis com- promising these structures, challenge diagnosis. Descrip- tions of such nerve variations are thus pertinent for anatomists, anesthesiologists, radiologists and surgeons. Conclusion The anatomical basis of BP collateral variations should be kept in mind, especially while performing surgical explo- ration, especially in the axillary and neck region and when interpreting clinical symptoms following trauma or tumor events. Being aware of the restrictiveness of this study's sample size, we have concluded from this study that: Almost half the evaluated plexus had collateral variations (47.1%); Subscapular nerves were the most varied structure, includ- ing the presence of an accessory nerve; Long thoracic nerve variations were present as were the absence of C5 or C7 involvement and late C7 union with C5–C6; Further studies are needed to confirm the existence of these variations in a larger sample of cadaver specimens. Abbreviations Brachial plexus (BP) Superior trunk (ST) Middle trunk (MT) Inferior trunk (IT) Anterior divisions (AD) Posterior divisions (PD) Acknowledgements We thank Javier Ariza Alvares (MD) for his contribution in acquiring data. References 1. Hollinshead WH: Anatomy for surgeons. Philadelphia, Harper & Row 3rd edition. 1982, 3:220-236. 2. Berry M, Bannister LH, Standring SM: Nervous system. In Gray's Anatomy 38th edition. Edited by: Williams PL. 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Sir Paul Nurse, Cancer Research UK Your research papers will be: available free of charge to the entire biomedical community peer reviewed and published immediately upon acceptance cited in PubMed and archived on PubMed Central yours — you keep the copyright Submit your manuscript here: http://www.biomedcentral.com/info/publishing_adv.asp BioMedcentral Journal of Brachial Plexus and Peripheral Nerve Injury 2007, 2:14 http://www.JBPPNI.com/content/2/1/14 Page 6 of 6 (page number not for citation purposes) 8. Erdogmus S, Govsa F: Mapping the course of long thoracic nerve. Neuroanatomy 2004, 3:2-7. 9. Benjamin K: Injuries to the brachial plexus: mechanisms of injury and identification of risk factors. Adv Neonatal Care 2005, 5:181-9. 10. Uzun A, Seeling LL Jr: A Variation in the formation of the median nerve: Communicating branch between the muscu- locutaneous and median nerves in man. Folia Morphol 2002, 60(2):99-101. 11. Gacek RR: Neck Dissection Injury of a BP Anatomical Variant. 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Surg Radiol Anat 2000, 22(3– 4):175-9. 24. Yan J, Wu H, Aizawa Y, Horiguchi M: The human suprascapular nerve belongs to both anterior and posterior divisions of the brachial plexus. Okajimas Folia Anat Jpn 1999, 76:149-55. 25. Tubbs RS, Loukas M, Shahid K, Judge T, Pinyard J, Shoja MM, Slappey JB, McEvoy WC, Oakes WJ: Anatomy and quantitation of the subscapular nerves. Clin Anat 2007:1. . incidence (38.7%), originating mostly from the posterior cord (21.1%). There must be full awareness of the origin of variation in collateral branches from the posterior aspect of the BP and their configuration. union at the second rib posterior to the axillary artery. They also found this union was at the first rib level posterior to the MT of the BP in 33% of cases. In addition, they also found that the. sub- scapular nerves originated from the axillary nerve and 12.3% from the thoracodorsal nerve (Fig 1). 50% of the upper subscapular nerves originated from the posterior division (PD) of the superior